Abstract--Pacific cod (Gadus macrocephalus) is an important
component of fisheries and food webs in the North Pacific Ocean and
Bering Sea. However, vital rates of early life stages of this species
have yet to be described in detail. We determined the thermal
sensitivity of growth rates of embryos, preflexion and postflexion
larvae, and postsettlement juveniles. Growth rates (length and mass) at
each ontogenetic stage were measured in three replicate tanks at four to
five temperatures. Nonlinear regression was used to obtain parameters
for independent stage-specific growth functions and a unified size- and
temperature-dependent growth function. Specific growth rates increased
with temperature at all stages and generally decreased with increases in
body size. However, these analyses revealed a departure from a strict
size-based allometry in growth patterns, as reduced growth rates were
observed among preflexion larvae: the reduction in specific growth rate
between embryos and free-swimming larvae was greater than expected based
on body size differences. Growth reductions in the preflexion larvae
appear to be associated with increased metabolic rates and the
transition from endogenous to exogenous feeding. In future studies,
experiments should be integrated across life transitions to more clearly
define intrinsic ontogenetic and size-dependent growth patterns because
these are critical for evaluations of spatial and temporal variation in
habitat quality.

**********

Fluctuations in the distribution and abundance of marine species
are highly influenced by climate-driven changes in ocean conditions
(Perry et al., 2005). In the Gulf of Alaska and Bering Sea,
oceanographic regimes linked to climate conditions (Hollowed et al.,
2001; Peterson and Schwing, 2003) occur across a variety of time scales,
from seasonal to multidecadal (Hunt and Stabeno, 2002). These climate
cycles have been linked to major shifts in the composition of valuable
groundfish communities (Anderson and Piatt, 1999). Imposed upon this
variation is the potential for longer-term climate changes, such as the
warming of surface waters and loss of sea ice (e.g., Hunt et al., 2002).
Such warming trends have already been observed in the Gulf of Alaska
(Royer and Grosch, 2006) and Bering Sea (Stabeno et al., 2007). The
response of individual populations and entire communities to
environmental forcing depends upon the physiological and behavioral
traits of individual species and the cumulative set of trophic
interactions between species (Freitas et al., 2007; Yatsu et al., 2008;
Hurst et al., 2010).

Spatial and temporal variation in temperature and prey availability
are considered to be primary drivers of growth and survival in early
life stages of fishes and their influence on recruitment has been
central to various generalized models of recruitment (see review by
Cowen and Shaw, 2002). The oscillating control hypothesis (OCH) states
that population production of groundfish in the Bering Sea is linked to
climate-driven patterns of prey production: cold winters with extensive
sea ice result in early, low-density blooms in cold water, resulting in
reduced survival of larvae (Hunt and Stabeno, 2002). Evaluation of the
OCH and predicting potential responses to future aspects of climate
change require detailed information on the temperature-dependent vital
rates of early life stages of fish (Kristiansen et al., 2007; Hollowed
et al., 2009; Rijnsdorp et al., 2009).

Pacific cod (Gadus macrocephalus) is a widespread marine species on
continental shelves throughout the eastern and western North Pacific and
Bering Sea. They are an important component of North Pacific and Bering
Sea fisheries and food webs. In recent years, U.S. landings of Pacific
cod trail only those of Alaska walleye pollock (Theragra chalcogramma)
and Atlantic and gulf menhaden (Brevoortia tyrannus and B. patronus)
(NMFS, 2008). Between 2002 and 2006, U.S. landings of Pacific cod
averaged 28 times those of Atlantic cod (Gadus morhua).

Despite the pervasive influence of temperature on all aspects of
biology and its potential linkage to recruitment patterns, there has
been little examination of the thermal ecology of Pacific cod. The
effects of temperature on the vertical distribution of larvae (Hurst et
al., 2009) and juveniles (Davis and Ottmar, 2009) have been examined.
Thermal effects on growth of Pacific cod has been examined in only the
very early life stages: development rates of eggs and prefeeding larvae
(Alderdice and Forrester, 1971; Laurel et al., 2008) have been examined
across a wide range of temperatures. In addition, B. J. Laurel (unpubl.
data) compared the effects of prey density on growth of preflexion
larvae at two temperatures. However, these studies are insufficient to
describe the functional response to temperature for larvae, and as of
yet, no data exist for later larval stages or juveniles.

In this article we describe the growth of early life stages of
Pacific cod as a function of temperature and body size. Separate
experiments were conducted with preflexion larvae, postflexion larvae,
and postsettlement juveniles. From these experiments and published data
on embryos, we determined the parameters for models of stage-specific
growth and for an integrated model of size- and temperature-dependent
growth. These functions will be used to evaluate the relative
contributions of temperature and feeding conditions to observed
variation in growth among wild Pacific cod (Folkvord, 2005; Hurst et
al., 2010).

Materials and methods

We determined the thermal sensitivity of growth rates at three life
stages: preflexion larvae, post-flexion larvae, and postsettlement
juveniles (Table 1). Growth rates at each ontogenetic stage were
measured in three replicate tanks at four to five temperatures,
encompassing the range likely to be encountered by fish in the Gulf of
Alaska and Bering Sea. Nonlinear regression was used to describe the
relationship between growth rate and temperature at each developmental
stage and to describe the combined effects of temperature and body size
on growth rates of early life stages.

Preflexion larvae

Two experiments were conducted to describe the growth of Pacific
cod larvae after hatching. In 2008, fish were reared at 2[degrees],
5[degrees], and 8[degrees]C to 36 days after hatching (dah). These data
were combined with data on fish reared under identical conditions to 35
dah at 3[degrees]C and 8[degrees]C in 2007 (B. J. Laurel, unpubl, data).
The 8[degrees]C treatment was conducted in both experiments to evaluate
potential differences in overall growth rates between years.

Fish for the larval growth experiments were reared in the
laboratory from eggs collected from spawning adults. Female and male
Pacific cod were caught by commercial jigging gear from spawning grounds
in Chiniak Bay, Kodiak Island, Alaska. The gametes were mixed and placed
into 4-L incubation trays at 4[degrees]C. At 24 hours after
fertilization, fertilized eggs were shipped in insulated containers to
the Alaska Fisheries Science Center's (AFSC) laboratory facilities
in Newport, Oregon. Eggs were transferred to flow-through 4-L plastic
trays and incubated at 4[degrees]C. Hatching occurred 19-22 days after
fertilization, after which larvae were transferred to larval rearing
tanks.

Experimental rearing tanks were 100-L cylinders with conical
bottoms and dark green walls. Water was supplied to the tanks at a rate
of 250 mL/min. Weak upwelling circulation was maintained in the tank by
positioning the in-flow at the bottom center of the tank and with light
aeration. Light regime during larval rearing was maintained at 12:12 h
light:dark; light was provided by overhead fluorescent bulbs at a level
of 6.7 [micro]E/[m.sup.2]s at the water surface.

Larval growth experiments were initiated by stocking rearing tanks
(maintained at the egg incubation temperature of 4[degrees]C) with 400
larvae which hatched over a 4-day period in the middle of the hatch
cycle. The last day that newly hatched fish were stocked into rearing
tanks is nominally referred to as experimental day 0. After the tanks
were stocked with fish, tank temperatures were adjusted to treatment
temperatures over 2 days. Larvae were reared on a combination of
rotifers (Brachionus plicatilis) enriched with Algamac 2000 (Aquafauna,
Hawthorne, CA; Park et al., 2006) and microparticulate dry food (Otohime
A, Marubeni Nisshin Feed Co., Tokyo). Rotifers were supplied at
densities of 4 prey/mL twice daily and dry food was provided 2-3 times
per day.

At periodic intervals, a subsample of 10 larvae was removed from
each tank to determine the mean size of larvae in the tank. For the 2007
experiments, six samples were drawn at 7-d intervals (starting on day
0). For the 2008 experiments, all tanks were sampled on days 0, 10, 23,
and 36. Sampled larvae were individually photographed under
magnification and measured from calibrated digital photographs using
ImagePro[R] (Media Cybernetics, Bethesda, MD) software. The
morphometrics used in these analyses were standard length ([L.sub.S])
and body depth of the myotome at the anus (D).

Dry weight of individual larvae was calculated using a two-step
model with [L.sub.S] and D developed from an independent collection of
similar size Pacific cod larvae reared in the laboratory under identical
conditions. These fish were individually photographed and dried on
preweighed foil at 68[degrees]C for at least 24 hours before
determination of dry mass (to 1.0 [micro]g) with a microbalance.
Fourty-four fish with [L.sub.S] of 5 to 11 mm were sampled periodically
over the first 45 dah. First, the body depth deviation ([D.sub.Dev]) was
calculated for each fish, reflecting variance in "condition"
from the equation

[MATHEMATICAL EXPRESSION NOT REPRODUCIBLE IN ASCII]. (1)

Individual dry mass ([M.sub.D] mg) was calculated from [D.sub.Dev]
and [L.sub.S] from the equation

[MATHEMATICAL EXPRESSION NOT REPRODUCIBLE IN ASCII]. (2)

These equations explained 97.8% of the variation in dry mass of
fish in the sample.

Growth rates were calculated for each replicate tank from the
increase in mean size of fish in measured subsamples. Growth in length
([g.sub.L], mm/d) and mass ([g.sub.M], /d) were calculated from linear
regression of mean length and In-transformed mass against sampling date.

Postflexion larvae

Growth rates of postflexion larvae were measured in a separate
experiment applying similar procedures. Experiments were established
with fish 50 dah, reared at 8[degrees]C under conditions similar to
those described above for preflexion larval experiments. Given the
variation in body size among cultured fish, each fish was assigned to
one of three size categories on the basis of visual estimation. This
sorting by size was done to minimize the potential for intracohort
cannibalism frequently observed in larval and juvenile gadids (Folkvord
and Ottera, 1993, Sogard and Olla, 1994). One group of 35-40 larvae from
each size category was assigned to each temperature treatment
(2[degrees], 4[degrees], 8[degrees], 11[degrees]C). In addition, a
sample of 15-20 fish from each size category was sacrificed to determine
initial size distributions.

After establishment of experimental groups (day 0), temperatures
were adjusted to target temperatures at a rate of 2[degrees]C per day.
Larvae were offered particulate food three to four times per day,
supplemented with enriched rotifers twice per day (first 20 d only). As
fish grew, larger size particulate food (up to 620 [micro]m) was
included in daily feedings. A subsample (7-10 fish) was drawn from the
8[degrees]C and 11[degrees]C treatments on day 18 and from the
2[degrees]C and 4[degrees]C treatments on day 24. The experiments were
ended and all surviving larvae were measured on day 32 for the
8[degrees]C and 11[degrees]C treatments and on day 45 for the
2[degrees]C and 4[degrees]C treatments. Lengths ([L.sub.S] and
[L.sub.T]) of all sampled larvae were measured with digital calipers
under a dissecting microscope and wet masses ([M.sub.W]) were measured
with a microbalance. Dry mass ([M.sub.D]) of each larvae was determined
after 48 hours in a drying oven at 50[degrees]C.

Growth rates were calculated from the increase in mean size of fish
in measured subsamples. Growth in length ([g.sub.L], mm/d) and mass
([g.sub.M], /d) were calculated from linear regression of mean length
and ln-transformed mass against sampling date.

Postsettlement juveniles

Age-0 Pacific cod were captured from Kodiak Island juvenile
nurseries in July 2008 with a 36-m beach seine. Fish were maintained for
at least 48 hours at the AFSC Kodiak Laboratory in ambient seawater
before shipment to the AFSC's laboratory in Newport, Oregon. Fish
were shipped overnight in insulated containers filled with seawater and
oxygen. Before use in laboratory experiments, fish were maintained in
1-m diameter round tanks with flow-through seawater maintained at
8-10[degrees]C. Fish were fed thawed krill and commercially available
pellets on alternating days.

The experiment was initiated by assigning fish-size categories
based on visual estimation and stocking fish into experimental tanks.
One tank of each size category (n=3) was assigned to each temperature
treatment (n=4; 12 tanks total). After establishment of experimental
groups, temperatures were adjusted to treatment temperatures
(2[degrees], 5[degrees], 8[degrees], and 11[degrees]C) and fish were
acclimated to the treatment temperature for 10 days.

Experimental tanks were 66 x 45.7 cm, filled to a depth of 23.2 cm.
During the experiment fish were fed thawed krill to apparent satiation
once per day. In addition, a gelatinized combination of squid, krill,
herring, commercial fish food, amino acid supplements, and vitamins was
provided three times per week. Lights were maintained on a 12:12 h
light:dark photoperiod for all experiments. Tanks were checked twice
daily for mortalities, and dead fish were removed, weighed, and
measured.

Growth rates were estimated by measuring ([L.sub.T] to 1 mm) all
fish in the experiment three times at 10-d intervals. To minimize stress
to small fish from repeated handling, wet masses were measured only at
the end of the experiment. Wet mass ([M.sub.W]) of individual fish at
earlier sampling points was estimated from regressions based on
measurements of fish collected but not used in this experiment and the
final experimental measurements.

Growth rates ([g.sub.L] and [g.sub.M]) of juvenile cod were
determined by regression of the measurements of fish length and
In-transformed mass against sampling date. In lieu of marking the 7-10
individual fish in each tank, we assumed that size rank was maintained
within each replicate tank during the experiment. Fish that died during
the experiment were not included in statistical analyses.

Growth models

For each of the life stages examined (egg-embryos, preflexion
larvae, postflexion larvae, juveniles), temperature-dependent growth
functions were estimated for growth in length and mass. For consistency
with the most commonly applied field measures of body size, growth rates
of embryos and larvae were expressed in terms of [L.sub.S] and
[M.sub.D], and juvenile growth rates as [L.sub.T] and [M.sub.W]. Growth
of postflexion larvae were expressed in both sets of measures.

For each life stage, a second-order polynomial function was fitted
to describe the relationship between temperature and growth rate. For
consistency in best-fit models, the second-order term was maintained,
although it was not statistically significant in some cases. For these
models, mean temperatures measured during the growth interval were
applied, rather than experimental target temperatures. The mean growth
rate measured in each replicate tank (n=3 per temperature) was used as
the level of observation.

In addition to stage-specific models, an integrated model of size-
and temperature-dependent growth (STDG) was developed (Folkvord, 2005).
Data for the model were derived from the above experiments on larvae and
juveniles and from previously published data on the hatching times and
sizes as a function of temperature (Laurel et al., 2008). Despite
representing easily identified discrete life stages with differing
habitats, data on growth of embryos before hatching were included with
posthatch data to clarify intrinsic patterns in potential growth rates
through the early life stages. Growth rates of prehatch embryos were
estimated from the size and age (days after fertilization) at hatching,
assuming [M.sub.D]=0.01 [micro]g and [L.sub.S]=0.0 mm at fertilization.
In order to standardize measures across life stages, measured [M.sub.W]
for juveniles was converted to [M.sub.D] and measured [L.sub.T] was
converted to [L.sub.S] on the basis of measurements of similarly size
fish (Hurst, unpubl, data).

The integrated STDG model was initially fitted with generalized
additive models (GAM) to examine the potential effects of nonlinear
interactions between mass and temperature on growth. These nonlinear,
nonparametric regression techniques do not require a priori assumptions
on the shape of the relationship between the dependent and independent
variables. After evaluation of potential interactions based on
evaluation of the generalized cross validation (GCV), a parametric model
formulation was selected that best represented patterns in the growth
data. Final models were fitted with parametric nonlinear regression in
Statistica (vers. 6.0, StatSoft, Tulsa, OK). This approach was
undertaken separately to provide STDG models for growth expressed in
mass ([M.sub.D]) and length ([L.sub.S]).

Results

Preflexion larvae

Mean size of larvae at hatch was slightly larger in the 2007
experiment than in the 2008 experiment ([L.sub.S] 5.16 vs. 4.90 mm;
[F.sub.[1,60]] = 45.4, P<0.001). However, there was no significant
difference among years in growth rates of preflexion larvae reared at
8[degrees]C ([g.sub.L] [F.sub.[1,41] = 1.52, P = 0.237; [g.sub.M]
[F.sub.[1,4]] = 3.90, P = 0.119), therefore data from the two
experiments were combined to describe the effect of temperature on
growth rate. In addition, there were no differences in growth rates
among replicate tanks at a given temperature (tested as the interaction
between day and tank on mean size, all P>0.05).

The sorting of fish by size before the establishment of
experimental groups produced significant differences in initial sizes of
experimental fish (group mean [L.sub.S] 14.02 to 16.10 mm; P=0.004).
Differences among size groups within temperature treatment were
generally maintained throughout the experiment but growth rates were
slightly higher in the small-size groups than the in large-size groups.
The effect of size group was significant for growth expressed as
[g.sub.M] ([F.sub.[2,6]]=15.7, P=0.004) but not for [g.sub.L]
([F.sub.[2,6]]=1.78, P=0.248).

Sorting of fish by size before the experiment resulted in
significant differences in initial size among replicates within
temperature treatments ([L.sub.T] [F.sub.[8,83]] = 9.46, P<0.001).
Differential growth during the temperature acclimation period resulted
in slight differences in initial sizes among temperature treatments
(treatment mean [L.sub.T] range: 48.8-51.8 mm; [F.sub.[3,83]]=2.70,
P=0.051). Although there were significant differences in growth rates
among tanks within temperature treatments, these were not consistent
across size groups, resulting in a significant interaction between
temperature and size group ([g.sub.M] [F.sub.[6,60]]=2.23, P=0.052;
[g.sub.L]: [F.sub.[6,60]]=2.34, P=0.042).

[FIGURE 1 OMITTED]

Growth in length and mass of juvenile Pacific cod was significantly
affected by rearing temperatures across the range examined (Fig. 3;
[g.sub.M] [F.sub.[3,6]]=59.3, P<0.001; [g.sub.L] ([F.sub.[3,6]]=26.7,
P<0.001). Growth rates at 11[degrees]C averaged 2.9 and 3.7 times
([g.sub.M] and [g.sub.L], respectively) greater than those observed at
2[degrees]C in similar size treatments. Best-fit functions describing
growth as a second-order function of temperature are shown in Table 2.

[FIGURE 2 OMITTED]

General growth model

Models of growth rates of early life stages of Pacific cod
indicated a discontinuity from strict allometric scaling during the
early larval stage. Growth rates of preflexion larvae were lower than
predicted based on a purely ontogenetic model incorporating growth-rate
data from embryos to settled juveniles. Therefore, two-stage models were
developed to describe growth in the egg stage separately from the
posthatch, free-swimming stages. Although growth was a function of both
temperature and body size, it was effectively modeled as the product of
independent functions of temperature and body size. There were no
significant interactions in the sense that the parameters of the
temperature-dependence function were not themselves a function of body
size. Therefore, embryonic and free-swimming stages shared a single
temperature-dependence function, differing only in elevation through
ontogeny (Fig. 4).

Growth rates of Pacific cod through the early life stages were
described by the equations

[MATHEMATICAL EXPRESSION NOT REPRODUCIBLE IN ASCII] (3)

and

[MATHEMATICAL EXPRESSION NOT REPRODUCIBLE IN ASCII] (4)

These equations explained over 88% of the observed variance in
growth rates of Pacific cod embryos to post-settlement juveniles
([g.sub.M] r=0.969; [g.sub.L] r=0.940). Analysis of residuals from these
models indicated greater variance at higher growth rates (small body
sizes and higher temperatures), but there were no trends in residuals in
relation to experimental temperature or body size that would indicate
significant departures from the model.

Discussion

Temperature is the dominant regulator of growth in early life
stages of fishes. In this study we examined the ontogenic pattern in
growth rate for early life stages of Pacific cod. We demonstrated a
deviation from strict allometric scaling, wherein growth rates after
hatching are lower than those predicted by body size allometry. We
determined parameters for temperature-dependent growth functions in
length and mass for specific life stages and for a unified STDG
function. These measures of growth potential can be used to evaluate the
biotic and abiotic factors regulating the growth and survival of early
life stages of Pacific cod in the wild (Folkvord, 2005; Hurst et al.,
2010).

Experiments

Because these experiments were conducted across a range of life
stages, many aspects of our experimental method had to be adapted for
each specific experiment, such as tank volume, prey type, and fish
density. However, the most significant differences in method between
egg-larval and juvenile experiments were the level of observation and
source of fish. To estimate growth rates of embryos and larvae,
subsamples of fish were drawn from a large tank population to determine
mean size at a specific age (Otterlei et al., 1999; Monk et al., 2008).
Change in mean size at age was then used to determine growth rate in
each replicate tank. With this approach, there is the potential for
size-selective mortality in the experiments to affect estimates of mean
growth rates. Such size-selective mortality is most commonly assumed to
be the result of predation (including cannibalism in single species
culture). However, such an effect is unlikely to have occurred in these
experiments: postflexion larvae were sorted by size before growth
experiments specifically to avoid potential cannibalism, and we saw no
evidence of cannibalism in the experiment (no larvae in samples with
fish in their stomachs). Because juvenile fish could be handled, they
were measured and returned to the tank and subsequently remeasured,
providing growth trajectories for individual fish. These individual
growth rates were then averaged to estimate mean growth rates of fish in
each tank (Hurst and Abookire, 2006; Wijekoon et al., 2009).

[FIGURE 3 OMITTED]

For experiments with eggs and larvae, we used the offspring of
field-caught spawning adults. In each year of experiments, gametes from
one or two females were mixed with those of three to five males.
Juvenile fish used in experiments were naturally produced and captured
after recruitment to juvenile nearshore habitats. Therefore, the genetic
diversity among experimental juveniles was significantly greater than
that found in experimental eggs and larvae. This difference in potential
genetic contributions to growth rates is not expected to have a
significant influence on the overall growth patterns described here
because maternal and genetic effects on growth have been shown to be
small in relation to environmental factors such as temperature (Benoit
and Pepin, 1999; Green and McCormick, 2005) and prey availability
(Clemmesen et al., 2003).

Ontogenetic patterns of growth

By combining results across life stages, we clarified ontogenetic
patterns in growth and length. With the exception of a departure during
the preflexion stage, growth patterns followed expected size-dependent
allometric patterns throughout much of the early development (Elliott
and Hurley, 1995). Growth in mass ([g.sub.M]) decreased with increases
in body size (Wootton, 1990) and growth in length ([g.sub.L]) was
constant across life stages. Although the constancy of [g.sub.L] across
a range of body sizes in early life stages has been noted in other
studies (Jones, 2002; Sigourney et al., 2008), those experiments have
not generally included the presettlement egg and larval stages
incorporated here. Interestingly, in Pacific cod, the general pattern of
across-stage similarity in [g.sub.L] extended from the egg-embryo stage
into the juvenile stage.

There was a significant departure from the expected ontogenetic
pattern in the preflexion larval period, most clearly observable in the
[g.sub.L] results. Measured [g.sub.L] among preflexion larvae averaged
only 41% of the rates measured for embryos, postflexion larvae, and
settled juveniles. Although less readily apparent, a similar departure
was observed in mass growth as the decline in [g.sub.M] between the
egg-embryo and preflexion larval stages was greater than expected from
allometric patterns accounting for the observed differences in body
size. In several studies on the growth of first-feeding gadids, higher
growth rates were reported for fish reared on copepods than on cultured
rotifers (Conceicao et al., 2010). Unfortunately, technical limitations
preclude rearing sufficient quantities of copepods for use in
experiments such as ours. For our study, larval Pacific cod were reared
on essential-fatty-acid--enriched rotifers, as the best of the
practicable prey alternatives. Therefore, it is possible that growth
rates of preflexion larvae are under-estimates of maximum potential
growth at this stage. However, the effect of prey type is insufficient
to completely explain the significantly lower growth rate observed at
this stage when compared to other stages. Further, similar observations
of reduced growth rates of fishes in the early posthatch phase have been
observed in several other studies. Experiments in which growth of
haddock (Melanogrammus aeglefinus; Martell et al., 2005) was tracked
through the egg--larva transition revealed a similar reduction in growth
associated with hatching. A similar pattern is apparent in Atlantic cod,
but without measurements of embryonic growth rates, the magnitude of
decline at hatching could not be determined (Otterlei et al., 1999;
Folkvord, 2005). However, these studies document a period of increasing
growth rates after hatching, followed by growth rate declines along
allometric expectations, indicating a similar overall pattern.

[FIGURE 4 OMITTED]

This reduction in growth during the egg--larva transition appears
to be the result of increased metabolic expenditures associated with
swimming in posthatch larvae and possibly a reduction in energy
available for growth associated with the transition from reliance on
endogenous energy stores to exogenous feeding (Torres et al., 1996;
Yufera and Darias, 2007). In Pacific cod, yolk reserves are depleted
3-12 dah, depending on water temperature (Laurel et al., 2008) and
stomach fullness increased through the first 28 dah (B. J. Laurel,
unpubl, data). The increase in growth rates after the preflexion
transitional feeding stage coincides with the onset of diel vertical
migrations (Hurst et al., 2009) and increased responsiveness to prey
(Colton and Hurst, 2010) among postflexion Pacific cod larvae. The
negative departure from an allometrically defined growth pattern after
hatching indicates that the first-feeding stage represents a
"critical period" in the early life history of Pacific cod and
that the consequences for recruitment of this low growth may be greater
at low temperatures (Kamler, 1992; Houde, 1996). In addition to
inclusion of embryo measurements into larval studies, future studies
with other species should encompass other major life history and habitat
transitions, such as metamorphosis and settlement in flatfishes
(Christensen and Korsgaard, 1999; Neuman et al., 2001) in order to
clarify the physiological basis of growth patterns and to determine
parameters for growth models.

Based on exploration of model structures for a unified STDG for
early life stages of Pacific cod, a two-stage model was developed. The
first stage described growth in the egg stage as a direct function of
water temperature. The second stage described growth in posthatch fish
as a function of water temperature and fish size. In addition to
providing the best fit to experimental data, this formulation is
logically consistent with the life history. Explicit discrimination
between life stages coincides with hatching, whereas the function
provides a continuous growth surface for all free-swimming stages. This
stage-independent model for posthatch fish provides more realistic
growth trajectories in modeling applications where fish are tracked over
multiple stages.

Applications of growth models

By quantitatively accounting for the influence of temperature
variation, laboratory-determined growth rates are being increasingly
used to evaluate factors regulating growth rates of fishes in the wild
(Folkvord, 2005; Rakocinski et al., 2006; Hurst et al., 2009). In these
analyses, "realized growth" expresses observed growth in the
field as a fraction of the potential growth at the encountered field
temperatures (Hurst and Abookire, 2006), with field growth rates
estimated from changes in mean size, otolith increment measures, or
biochemical measures (RNA:DNA). In these studies it is important to
recognize that growth rates of individuals are determined by both
genetic and environmental factors. Growth models from laboratory
experiments generally describe mean growth of a representative
population under optimal foraging conditions, which should not be
mistaken for the maximum growth rates that would be observed for the
fastest growing individual. Therefore, field growth rates should be
similarly expressed as a population mean rather than at the individual
level. Realized growth rates near 100% indicate that growth rates in the
population are directly limited by ambient temperature variation. In
studies of juvenile flatfishes, this temperature regulation of growth
has been referred to as the "maximum growth/optimal food
condition" hypothesis (Karikiri et al., 1991; van der Veer and
Witte, 1993). Conversely, realized growth rates significantly below 100%
indicate that growth is regulated by nonthermal environmental factors
such as light regime or prey availability (Buckley et al. 2006;
Kristiansen et al., 2007; Hurst et al., 2009).

Unfortunately, many studies of growth rates in fishes are conducted
over a limited size range and usually within a single life stage.
Therefore, these data have limited application where growth rates of
wild fish are tracked over longer time periods or through early life
history stage transitions. For example, in evaluating the mechanisms
responsible for variation in survival and recruitment, it is critical to
determine whether growth reductions among wild fish are due to inherent
physiologically based patterns (as appears in post-hatch gadids) or are
imposed by an unfavorable growth environment (Jones, 2002). In another
application of laboratory data to field studies, the back-calculation of
hatch dates from estimated temperature-dependent growth rates (Lanksbury
et al., 2007) could be biased if ontogenetic patterns in growth
variation are not accounted for.

Conclusion

Growth variation in early life stages can result in body-size
variation that persists over time and has significant implications for
the survival and recruitment of marine fish larvae (Houde, 1996; Jones,
2002). Successful evaluation of the biotic and abiotic factors
regulating this underlying variation in growth requires detailed
information on the size- and temperature-dependency of potential growth
throughout the early life history. Identifying the intrinsic patterns in
growth-rate allometry and reductions among preflexion larval Pacific cod
was based on the integration of experimental data on embryos and
larvae,--stages generally considered in isolation from each other. We
suggest that data on embryos be routinely incorporated with larval data
to clarify ontogenetic and temperature-dependent growth patterns in the
early life history stages of fish.

The views and opinions expressed or implied in this article are
those of the author (or authors) and do not necessarily reflect the
position of the National Marine Fisheries Service, NOAA.

Acknowledgments

We thank T. Tripp, M. Spencer, and B. Knoth for assistance with
fish collection and shipping. Staff and students in the Fisheries
Behavioral Ecology Program, including L. Copeman, S. Haines, M. Ottmar,
P. Iseri, A. Colton, L. Logers, E. Seale, and J. Scheingross assisted
with various laboratory experiments. S. Munch, L. Tomaro, A. Stoner, and
three anonymous reviewers provided helpful comments on earlier versions
of this manuscript. This research was supported in part by a grant from
the North Pacific Research Board (no. R0605). This is publication no.
248 of the North Pacific Research Board.